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ORIGINAL ARTICLE

Evaluation of Allergic Fungal Occurrence in Patients with Nasal Polyps

ABDUR REHMAN, FAISAL RAFIQ, ATHAR ADNAN UPPAL*

ABSTRACT

Aim: To evaluate allergic occurrence in patients with nasal polyps. Methods: This was a prospective descriptive study, conducted at ENT Department of Nawaz Sharif Social Security Hospital Multan Road Lahore , from January 2013 to June 2015. A total of 125 patients with nasal polyps were examined and performed followed by histopathology and culture examination of surgical specimens. Results: Allergic fungal sinusitis (AFS) was found in 28/125 (22.4%) nasal patients. In 28 cases of allergic fungal sinusitis, mean age was 30 years. Majority of patients (67.8%) were in the age range 20 – 40 years. Male to female ratio was 1.4:1. Most (53.5%) of AFS patients belonged to lower social class. Concomitant was noted in 06 (21.4%) patients. Conclusion: Allergic fungal sinusitis is common aetiology seen among nasal polyp patients. Slightly more than one fifth of cases with nasal polyp (22.4%) had AFS in this study, While treating chronic rhinosinusitis patients, this disease entity must be kept in mind. AFS was seen to effect mainly young adults and middle aged poor people living in hot humid conditions. Aspergillus was the commonest organism responsible for AFS. Results are good if it is diagnosed early and treated properly. Keywords: Allergic fungal sinusitis (AFS), Nasal polyp, Allergic mucin.

INTRODUCTION elevated total and fungus specific IgE Allergic fungal sinusitis is an allergic reaction of the concentration5,10. The involved sinuses contain brown sinonasal mucosa to aerosolized environmental 1 or greenish black material,which has been called fungal allergens in an immunocompetent person . allergic mucin, and intact and degenerating Safirstein in 1976 described a clinical condition in , Charcot Leyden crystals, cellular debris, which there were nasal polypi and crust formation and sparse fungal hyphae4,5,11. and sinus culture producing aspergillus, having The diagnosis of AFS is primarily based on similar histopathological findings to allergic 5 2 histopathologic findings. Patients with AFS bronchopulmonary aspergillosis (ABPA) . Allergic commonly present with chronic rhinosinusitis with fungal sinusitis (AFS) was first described by Millar in nasal polyps, inhalant atopy/ IgE mediated 1981 as “allergic aspergillosis”. A subsequent study 3 hypersenstivity, elevated total serum immunoglobulin was done by Robson and colleagues in 1989 and E (IgE), eosinophilia and sinus obstructing they introduced the term "allergic fungal sinusitis". inspissates of a characteristic extramucosal “peanut Allergic fungal sinusitis is associated with nasal 4 butter” or “axle grease” rich material called polyps in every case. The overall incidence of allergic mucin4,5, ,Allergic mucin typically cultures allergic fungal sinusitis is estimated at 5% to 10% of positive for fungi but the diagnosis of AFS is made all patients with chronic rhinosinusitis and nasal 4,5,12 1,4,5 6 even if culture is negative . Up to 13% of AFS polyps . The geographic and social factors appear sinus fungal cultures prove to be negative in AFS to have a significant impact on the incidence and confirmed on histopathology9. Allergic mucin is frequency of allergic fungal sinusitis, typically patient responsible for characteristic CT scan finding of is a young adult from warm regions with high 1,4,7 8 central area of hyperattenuation in the sinus cavity humidity and belonging to poor social class . which is one of the diagnostic criteria for AFS2,4. It is a non- invasive disease, representing an allergic Mainstay of treatment of AFS is both medical hypersensitivity response to the presence of extra 9 and surgical debridement of polypi and allergic mucosal fungi within the sinus cavity. Patients often mucin1,7. External radical approaches were used have asthma, allergic , eosinophilia, and an previously but now used rarely, these days we use ------tissue preserving endoscopic approach.4,5 The use of Deptt. of ENT Nawaz Sharif Social Security Teaching Hospital, postoperative oral corticosteroids1,2,5 and aggressive Multan Road Lahore 13 *Deptt. of ENT FMH College of and Lahore antiallergic is also recommended to Correspondence to Dr. Abdur Rehman, Assistant Professor Email: decrease recurrence after surgery4,7,14. Other [email protected] Cell: 0300-4358054 therapeutic options available include allergen

P J M H S Vol. 9, NO. 3, JUL – SEP 2015 875 Evaluation of Allergic Fungal Sinusitis Occurrence in Patients with Nasal Polyps avoidance measures, oral , intranasal RESULTS , leukotriene receptor antagonists, and allergen immunotherapy4,11. Role of systemic or local During the study period, we happened to manage antifungal treatment is limited and controvertial4,5. 125 patients with nasal polyps, among them, 85 were The purpose of this study was to find out male and 40 female patients, having mean age of 33 frequency and clinical/demographic characteristics of years (range 09 - 82 years). The patients with allergic allergic fungal sinusitis in patients with nasal polyps fungal sinusitis were 28(22.4%) and remaining 97 treated surgically in this part of the world. were found to have some other cause for the nasal polyps. Among 28 cases of allergic fungal sinusitis MATERIAL AND METHODS cases, proved on final histopathology, mean age was 30 years (range 11-48 years). Male to female ratio This was a prospective, cross-sectional descriptive was 1.4:1(Table 1). study, conducted at Nawaz Sharif Social Security Hospital (NSSSH) Lahore from January 2013 to June Table 1: Gender among patients with nasal polyps: 2015. NSSSH is a tertiary care and teaching hospital Gender AFS* %age Non AFS** %age for University College of Medicine, University of Male 17/28 60.7 68/97 70.1 Lahore. Female 11/28 39.3 29/97 29.9 The study subjects included 125 patients who *allergic fungal sinusitis presented with nasal polyps at NSSSH during the **non-allergic fungal sinusitis period under study. Both male and female patients Table 2: Age and gender distribution of patients with having nasal polyps were included in the study. We allergic fungal sinusitis (n=28). excluded those particular patients from the study who Age (Years) Male Female Total had friable nasal mass (bleed to touch) or did not 10-19 03 02 05 give consent for surgery and histopathlogy. 20-29 05 04 09 These patients were received through casualty, 30-39 06 04 10 Out-patient department (OPD) and as referral from 40-48 03 01 04 other departments. A detailed history was taken; Total 17 11 28 thorough examination of ENT and other systems was carried out by using well illuminated head light and Majority of patients (67.8%) belonged to the group of nasal speculum followed by fibroptic flexible or rigid patients in the age range 20 – 40 years with mean endoscope for detailed inspection. Laboratory age 30.64±S.D 6.03 years (Table 2). investigations included complete blood count, blood urea etc. Besides baseline investigations CT scan Table 3: Social history of the patients (n=28). and MRI of and were Status n %age performed to know the exact site and extent of Lower Socioeconomic Class* 15 53.5 disease. A well informed consent was taken. All the Middle Socioeconomic Class** 08 28.6 patients underwent nasal polypectomy under general Upper Socioeconomic Class*** 05 17.9 or local anesthesia, mainly by doing endoscopic Rural 20 71.4 sinus surgery and in few cases by external Urban 08 28.6 ethmoidectomy. Note: *Patients having income After surgery collected material which included ≤ Rs: 15,000/ month. together with inflamed tissue and pieces of **Patients having income Rs: 15,000–45,000/ month. polyps was divided into two parts. One part was kept ***Patients having income in sterile tube containing normal saline solution for ≥ Rs: 45,000 / month. direct microscopic examination. The remaining part of surgical specimen was kept in another bottle Majority (53.5%) belonged to low socioeconomic containing formalin and both the specimens were class and from rural (71.4%) area. Unilateral nasal sent to department for histopathological polyps were more frequently seen (64.2%) as and direct microscopic examination. These patients compared to bilateral nasal polyps (35.8%).There were put on topical and oral steroids therapy were 6(21.4%) patients with proptosis, and 3(10.7%) postoperatively and they were followed up for one cases complained of blurred vision whereas 6(21.4%) year. The data was collected using a pre-tested, patients were found to have concomitant asthma structured proforma prepared for the purpose and (Table 4). SPSS version 17 was used for analysis.

876 P J M H S Vol. 9, NO. 3, JUL – SEP 2015 Abdur Rehman, Faisal Rafiq, Athar Adnan Uppal

Table 4: Clinical presentation in allergic fungal sinusitis literature reveals that incidence of AFS is higher in Clinical features. n %age warm regions with relatively high humidity2,4,20. Bilateral polyps. 10 35.8 Any gender may be affected; however in this Unilateral polyps. 18 64.2 study males were affected more which is like the Nasal obstruction 28 100 result of Bashir21 who had male: female ratio of 1.4:1 Proptosis 06 21.4 while it is different from Baloch ZA18, where females Blurred Vision 03 10.7 were predominant and Karthikeyan22 who had equal Asthma 06 21.4 sex ratio. AFS may affect any age patient, but in our

study most of patients (67.8%) with AFS were in age All patients had surgical treatment. Out of 125, 28 range of 20 – 39 years which is in agreement with (22.4%) patients were reported as non-invasive 23 Shrestha’s study who had 60% patients belonging allergic fungal sinusitis on final histopathology. For to middle age group. It may be that people in middle patients ultimately diagnosed as allergic fungal age are more prone to the risk factors of environment sinusitis (AFS), functional endoscopic sinus surgery as they have more active life. In this study most of was the procedure performed in 20/28 (71.4%) cases the patients (53.5%) belonged to low socioeconomic while in 08(28.6%) cases external fronto- 21,24 class which is comparable to national studies . It ethmoidectomy was required (Table: 5). seems that socioeconomic status of person may

have some association with AFS. Table 5: Surgical approaches used in allergic fungal sinusitis (n=28) As far as symptomatology is concerned, in this Procedures n %age study all the patients with AFS were found to have nasal obstruction (100%) followed by nasal discharge External frontoethmoidectomy 08 28.6 (86%), which are similar to the results of Thahim8, Functional endoscopic sinus surgery. 20 71.4 where the commonest presenting symptom was Total 28 100 nasal obstruction (100%) followed by nasal discharge Culture of surgical material grew aspergillus in (90%) and postnasal drip (90%). The disease was 18(64.3%) cases whereas there was no fungal unilateral in 64.2% and in 35.8% it was bilateral. growth in 10(35.7%) cases. Remaining 97 patients While on presentation 6 (21.4%) cases with AFS had were diagnosed as non-allergic fungal sinusitis / proptosis. In this study patients having AFS and simple inflammatory ethmoidal nasal polyps. concomitantly asthma were 21.4% which is less than study of Telmesani19 who had 27.5% patients and 23 DISCUSSION Shrestha who reported 34% patients with associated asthma. Allergic fungal sinusitis has become well known CT scan showed in majority of patients with medical condition. The incidence of AFS has been AFS, involvement of more than one sinus with areas reported in international literature to be approximately of attenuation surrounded by an area of hypodensity. 6 - 7% of chronic rhinosinusitis cases treated by Culture of surgical material grew aspergillus in 18 surgery.2,15 This study was done with the purpose to (64.3%) cases with AFS. This was within culture yield evaluate this entity in our region as locally, not much range of 60-100% reported in other international work has been done on the subject. studies4,17. It is important to realize that diagnosis of We found AFS in 22.4% of the patients with AFS is not established or eliminated on the basis of nasal polyps in this study, this is higher when the results of fungal cultures4. compared with some of the local studies16,17. Akhtar Mainstay of treatment of AFS is surgical mostly MR16 reported 14% frequency whereas Irshad-ul-Haq endoscopic sinus surgery. We had done endoscopic M17 reported 11% frequency of AFS among patients surgery in 71.4% of the cases. External with nasal polyps. Another local study by Baloch ZA18 frontoethmoidectomy was done in 08(28.6%) cases reported 38% frequency of AFS, which is quite high where the disease was extensive, extending into orbit compared to our results. Internationally Telmesani or intracranially. LM19, in his study found AFS in 12.1% of nasal polyp Oral prednisolone in dose of 0.5 mg/kg body patients. These results show that there is great weight was used for 03 months and topical nasal variation in AFS frequency among patients with steroids for 6 months. Three monthly follow up was chronic sinusitis with nasal polyp and it’s increasing arranged up to a period of 1 year after surgery. when compared to previously reported incidence of Recurrence was reported in 4(14.3%) cases in our 7% in international literature2,15. Geographic factors study, which is within the range of 10 to 100 % seem to influence the incidence of AFS. Review of recurrence, reported in literature4.

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CONCLUSION and sinonasal polyposis. Bangladesh J Otorhinolaryngol 2011, 17: 117-120. Allergic fungal sinusitis is common aetiology seen 12. Javer AR, Genoway KA, Gervais M ,et al. Fungal among nasal polyp patients. Slightly more than one cultures in patients with allergic fungal rhinosinusitis: fifth of cases with nasal polyp (22.4%) had AFS in Improving the recovery of potential fungal pathogens in this study. While treating chronic rhinosinusitis the Canadian laboratory. J Otolaryngol 2007; 36 (1): 1- patients, this disease entity must be kept in mind. 5. 13. Challa S, Uppin SG, Hanumanthu S, Panigrahi MK, AFS was seen to effect mainly young adults and Purohit AK, Sattaluri S et al. Fungal rhinosinusitis: a middle aged poor people living in hot humid clinicopathological study from South India. European conditions. Aspergillus was the commonest organism Archives of 2010; 267: 1239- responsible for AFS. Results are good if this disease 1245. is diagnosed early and treated properly. 14. Ikram M, Abbas A, Suhail A, Onali MA, Akhtar S, and Iqbal M, Management of allergic fungal sinusitis with REFERENCES postoperative oral and nasal steroids: A controlled study Ear Nose Throat J. 2009;88(4):E08 1. Lester D.R. Thompson, MD Allergic fungal sinusitis Ear 15. Lanza DC, Dhong HJ, Tantilipikorn P, Tanabodee J, Nose Throat J. 2011;90(3):106-107 Nadel DM, Kennedy DW. Fungus and chronic 2. Kumar N, Berry V. Allergic fungal sinusitis JK Science, rhinosinusitis: from bench to clinical understanding. Journal of & Research, 2008; Ann Otol Rhinol Laryngol 2006; 196 (suppl) : 27-34. 10(1):5-8. 16. Akhtar MR, Ishaque M, Saadat ullah. Aetiology of 3. Robson JM, Hogan PG, Benn RA, Gatenby PA. nasal polyp. Pak J Otolaryngol 2004; 20: 9-11. Allergic fungal sinusitis presenting as a paranasal 17. Irshad-ul-Haq M, Farooq M, Qadri SH. Prevalence of sinus tumour. Aust N Z J Med 1989; 19:351-3. allergic fungal sinusitis among patients with nasal 4. Gupta AK, Shah N, Kameswaran M, Rai D, Janakiram polyps. JSZMC 2014;5(4):690-692. TN, Chopra H, et. al.Allergic Fungal Rhinosinusitis. 18. Baloch ZA, Ahmad AN, Mahmood Z, et al. Frequency Clin Rhinol An Int J 2012;5(2):72-86. of Allergic Fungal Sinusitis in Patients with Nasal 5. Glass D, Amedee RG. Allergic Fungal Rhinosinusitis: Polyposis and its Causative Species. Pakistan Journal A Review .The Ochsner Journal 2011; 11: 271–275. of Otolaryngology 2010; 26:76-77. 6. Ferguson BJ, Barnes L, Bernstein JM, Brown D, Clark 19. Telmesani LM. Prevalence of Allergic fungal sinusitis CE 3rd, Cook PR, et al. Geographic variation in among patients with nasal polyps. Ann Saudi Med allergic fungal rhinosinusitis. Otolaryngol Clin North 2009;29:212-214 Am 2000; 33:441-9. 20. Schubert MS. Allergic fungal sinusitis: 7. Shockley R, Roy S, Allergic fungal rhinosinusitis in pathophysiology, diagnosis and Management. Medical children Ear Nose Throat J. 2012; 91(7):280-281. Mycology 2009; 47: 324-330. 8. Thahim K, Jawaid MA and Marfani MS. Presentation 21. Bashir H, Khawar A and Hussain A. Comparison of and management of allergic fungal sinusitis. JCPSP efficacy of levocetrizine and fexofenadine in patients 2007; 17(1): 23-27. with symptomatic . Pakistan Journal of 9. Azar S, Mansour B, Parivash K and Babak B. Fungal Otolaryngology 2011; 27: 66-68. Rhinosinusitis in Hospitalized Patients in 22. Karthikeyan P and Coumare N. Incidence and Khorramabad, Iran. Middle East Journal of Scientific Presentation of Fungal Sinusitis in Patient Diagnosed Research 2011; 7: 387-391. with Chronic Rhinosinusitis. Indian J Otolaryngol Head 10. Soontrapa P, Larbcharoensub N, Luxameechanporn T, Surg. 2010; 62: 381–385. Cheewaruangroj W, Prakunhungsit S, 23. Shrestha S, Kafl e P, Akhter J, Acharya L, Khatri R, KC Sathapatayavong B et al. Fungal Rhinosinusitis: a T. Allergic Fungal Rhinosinusitis in Chronic Retrospective Analysis of Clinicopathologic Features Rhinosinusitis. J Nepal Health Res Counc 2011; 9: 6- and Treatment Outcomes at Ramathibodi Hospital. 9. Southeast Asian J Trop Med . 2010; 41: 24. Khan AR, Ali Farman, Din SE, Khan NS and Dawar A. 442-49. Frequency of Allergic Fungal Chronic Rhinosinusitis. 11. Kamal MS, Ahmed KU, Humayun P, Atiq T, Hossain A Pak J of Otolaryngol 2011; 27: 12-14. and Rasel MA. Association between allergic rhinitis

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